Botanical Sources and Sugar Concentration of the Nectar Collected by Two Stingless Bee Species in a Tropical African Rain Forest*

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Botanical Sources and Sugar Concentration of the Nectar Collected by Two Stingless Bee Species in a Tropical African Rain Forest* Apidologie 38 (2007) 110–121 110 c INRA/DIB-AGIB/ EDP Sciences, 2007 DOI: 10.1051/apido:2006051 Original article Botanical sources and sugar concentration of the nectar collected by two stingless bee species in a tropical African rain forest* Robert Ka, b a Faculty of Biology, Department of Behavioural Biology, Tropical Bee Research Unit, PO Box 80.086, 3508 TB Utrecht, The Netherlands b Permanent Address: Department of Forest Biology and Ecosystems Management, Faculty of Forestry and Nature Conservation, Makerere University, PO Box 7062, Kampala, Uganda Received 3 January 2005 – Revised 15 October 2005 – Accepted 10 August 2006 Abstract – Nectar foraging by species of two stingless bees was studied in an African tropical rain forest. Both species Hypotrigona gribodoi (2–3 mm) and Meliponula ferruginea (6 mm) collected nectar with a wide range of sugar concentration (H. gribodoi: 14.2–67.4%; M. ferruginea: 9.1–63.4%). H. gribodoi col- lected nectar of higher sugar concentration than M. ferruginea. Factors that influenced sugar concentration of collected nectar included botanic origin of the nectar, bee species, bee colonies, month of year, time of day and the local environment. Sugar concentration increased gradually from 0700 h to a peak at 1300 h and declined thereafter. H. gribodoi collected nectar from more diverse plant species than M. ferruginea. Sugar concentration for both bee species was higher during the dry season than the rainy season. Although the above factors may explain part of the variation in the sugar concentration of nectar, additional explanations lie in the behavioural differences among the bee species. nectar concentration / nectar sources / Calliandra calothyrsus / foraging behaviour / Budongo Forest Reserve 1. INTRODUCTION qualities and quantities presented by plants (Roubik, 1989; Biesmeijer et al., 1999b). Several species of stingless bees can oc- Flower visitors can differentiate between the cur sympatrically and their diets partly over- amount of nectar in flowers, its sugar concen- lap permitting access to the same resources tration, and its composition in sugars, amino by many colonies (Sommeijer et al., 1983; acids and lipids (Baker and Baker, 1975, 1983; Roubik et al., 1986; Kleinert-Giovanini and Opler, 1983; Roubik and Buchmann, 1984; Imperatriz-Fonseca, 1987; Ramalho et al., Roubik et al., 1995; Biesmeijer and Ermers, 1989; Ramalho, 1990; Roubik et al., 1995; 1999). Kajobe and Roubik, 2006). The overlap in diet can lead to competitive interactions (Hubbel Honey bees have a preference mainly for and Johnson, 1977, 1978; Roubik and Aluja, those plants that provide a better reward, that 1983; Roubik, 1989). The competition for nec- is the largest amount of pollen, or nectar, or tar can result in the evolution of not only both, those having more concentrated nectar, morphological adaptations of both plants and and those that have not been foraged on pre- animals but also in a wide range of nectar viously by other bees (Roubik, 1989). Factors that cause variation in harvested nectar sugar Corresponding author: R. Kajobe, concentration include the botanical origin of [email protected] nectar, local climate, as well as behavioural * Manuscript editor: B. Vassière and J. Pierre differences among bee species and among Article published by EDP Sciences and available at http://www.edpsciences.org/apido or http://dx.doi.org/10.1051/apido:2006051 Nectar sources and sugar concentration for African stingless bees 111 Figure 1. Location of the Budongo Forest Reserve (DRC = Democratic Republic of Congo). colonies within the same species (Biesmeijer Studies are very limited on the floral origin et al., 1999b). These authors concluded that of nectar collected by African stingless bees. the variation of climatological conditions be- There has been no major study to fully explain tween patches might lead to heterogeneous the nectar foraging ecology of social bees in nectar rewards. African tropical rain forests. The patterns and ecological impact of floral choice and foraging Spatial and temporal niche differentiation behaviour of social bees in this environment between sympatric stingless bee species can are largely unknown. This study was there- arise by differences in bee morphology, for ex- fore aimed at answering the following ques- ample with body size, colour and mouth parts tions: what are the important nectar sources of (Biesmeijer et al., 1999a). Resource partition- stingless bees in the Budongo forest reserve? ing can also be the result of behavioural dif- What is their diversity? What factors influence ferences among bee foragers, for example the the sugar concentration of collected nectar, in timing of the foraging activity, the ability to particular is there an effect of the bee species recruit, the intrinsic collecting behaviour, ag- on the concentration of the nectar collected? A gressiveness, and the food selection (Frankie comparison between honey bees and stingless et al., 1976; Villanueva, 1994). Temporal re- bees was made in an effort to understand the source partitioning was described by Frankie ecology of their nectar foraging behaviour. et al. (1976) who found that the species com- position of bee fauna foraging on a particular flower patch changed over the course of a day, 2. MATERIALS AND METHODS thus suggesting that differences in the timing of foraging may help to avoid direct compe- 2.1. Study site tition among species at flowers. In that study, they noted a tendency for larger bees to for- The main study was conducted in the Budongo age earlier in the day compared to the smaller Forest Reserve (BFR), which is a tropical rain for- species. est located in mid-western Uganda. It is an outlier of 112 R. Kajobe the great Ituri forest of the Democratic Republic of Nectar was collected from foragers by forcing the Congo (Fig. 1). It covers an area of 825 km2,mak- bees to expel their crop load into a 20 µL capillary ing it Uganda’s biggest forest reserve (Hamilton, tube for the small bee, H. gribodoi and 50 µLfor 1984); 53% of it is continuous forest cover while M. ferruginea. In the case of H. gribodoi, samples the remaining comprises grassland communities. It from 2–3 bees were occasionally combined to ob- is located east of the Western rift valley escarp- tain more reliable sugar concentration values. Con- ment and Lake Albert between 1◦35’ and 1◦55’ centration of sugar (actually total dissolved solids) N, and 31◦18’ and 31◦42’ E (Howard, 1991). The in the nectar was measured with a hand refractome- forest lies at an average altitude of 1100 m (mini- ter corrected for ambient temperature (results ex- mum 750 m and maximum 1250 m) above sea level pressed in g per 100 g of solution). Bees carrying (Eggeling, 1947). loads with less than 5% in sugar concentration were ignored because they probably consisted mainly of water foragers (Roubik and Buchmann, 1984). Data 2.2. Bee colonies on ambient temperature was taken at each time of nectar collection. We used four natural nests of two stingless bee species, two colonies of Hypotrigona gribodoi and two of Meliponula ferruginea. These two species 2.4. Identification of nectar and pollen were selected because they represent the two gen- sources era of stingless bees that have been identified in Uganda. The colonies were located at most 80 m Nectar foragers carried pollen of different apart in various tree cavities close to the border of colours on different parts of their bodies. These the forest. The stingless bees were identified based pollen grains adhering to the body of the bees on Eardley (2004) and their identity was confirmed were sampled by trapping the bee with glycerine by David W. Roubik at Smithsonian Tropical Re- jelly and we analysed this pollen to identify the search Institute. Measurement of the bee sizes (dry nectar sources used by the bees. We obtained a body length) was recorded in the Royal Museum wide variety of samples by selectively sampling for Central Africa, Tervuren, Belgium, using an oc- foragers from each visually distinguishable pollen ular micrometer on a stereoscopic microscope. The colour type. Such a sampling method can cause smaller bee species, H. gribodoi (2–3 mm) is pale a slight overestimation of the diversity in nectar in colour. Two morphs of M. ferruginea (6 mm), diet (Biesmeijer et al., 1999b). Several representa- one black and the other brown have been identified tives of each colour of pollen were acetolysed and in Uganda. They were previously called Meliponula mounted in glycerine jelly for microscopic exam- erythra, but are now regarded as species synonyms ination (Sawyer, 1981). The colour and amount of (Eardley, 2004). The brown form is the one that ex- the pollen was recorded. Most slides contained only ists in Budongo forest reserve and was therefore one type of pollen and slides that contained more used in this study. than one type were not included in our analysis. The different pollen types were identified by mak- ing use of our reference collection and by consult- 2.3. Sampling and analysis of nectar ing Hamilton (1972). A nectar source was referred collected by H. gribodoi and to as a major source if it contributed at least 30% of M. ferruginea the samples from one colony during a day of obser- vation. All other sources were referred to as minor From March to August 2002, nectar samples sources. were taken once a week from 10 returning foragers per colony, five times a day at 0600–0700 h, 0900– 1000 h, 1100–1200 h, 1300–1400 h and 1500– 2.5. Nectar collection from Calliandra 1600 h local time. The methods used were similar to calothyrsus by stingless bees and those used by Biesmeijer et al. (1999b). At the nest Apis mellifera entrances, returning nectar foragers were caught with a net.
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